Pivotal roles of phyllosphere microorganisms at the interface between plant functioning and atmospheric trace gas dynamics.

Bringel F, Couée I - Front Microbiol (2015)

Bottom Line:
The phyllosphere, which lato sensu consists of the aerial parts of plants, and therefore primarily, of the set of photosynthetic leaves, is one of the most prevalent microbial habitats on earth.Recent -omics studies have opened fascinating opportunities for characterizing the spatio-temporal structure of phyllosphere microbial communities in relation with structural, functional, and ecological properties of host plants, and with physico-chemical properties of the environment, such as climate dynamics and trace gas composition of the surrounding atmosphere.This review will analyze recent advances, especially those resulting from environmental genomics, and how this novel knowledge has revealed the extent of the ecosystemic impact of the phyllosphere at the interface between plants and atmosphere.

ABSTRACTThe phyllosphere, which lato sensu consists of the aerial parts of plants, and therefore primarily, of the set of photosynthetic leaves, is one of the most prevalent microbial habitats on earth. Phyllosphere microbiota are related to original and specific processes at the interface between plants, microorganisms and the atmosphere. Recent -omics studies have opened fascinating opportunities for characterizing the spatio-temporal structure of phyllosphere microbial communities in relation with structural, functional, and ecological properties of host plants, and with physico-chemical properties of the environment, such as climate dynamics and trace gas composition of the surrounding atmosphere. This review will analyze recent advances, especially those resulting from environmental genomics, and how this novel knowledge has revealed the extent of the ecosystemic impact of the phyllosphere at the interface between plants and atmosphere. Highlights • The phyllosphere is one of the most prevalent microbial habitats on earth. • Phyllosphere microbiota colonize extreme, stressful, and changing environments. • Plants, phyllosphere microbiota and the atmosphere present a dynamic continuum. • Phyllosphere microbiota interact with the dynamics of volatile organic compounds and atmospheric trace gasses.

Mentions:
Pioneering studies on microbiota in clouds have shown the presence of prevalent bacteria that are common with phyllosphere microbiota, thus suggesting that at least some epiphytic microorganisms are adapted to the conditions of the troposphere (DeLeon-Rodriguez et al., 2013; Šantl-Temkiv et al., 2013). Tropospheric microorganisms are likely to act as water condensation or nucleation centers during cloud formation and to be involved in global carbon cycles through metabolization of the organic compounds that are present in clouds (Vaïtilingom et al., 2013). Moreover, epiphytic microorganisms may constitute the major source of airborne bacteria, including ice nucleation-active (INA) bacteria. These bacteria mainly belong to the order of Gammaproteobacteria and possess common INA proteins encoded by ina genes that were qPCR quantified and estimated to reach up to 108ina genes per g of fresh weight in the foliage of cereals (Lindemann et al., 1982; Hill et al., 2014). The presence of INA proteins may also contribute to bacteria dissemination processes via deposition on cloud droplets. There may thus be strong links between phyllosphere microbiota and cloud microbiota (Figure 5) with important implications for climate regulation.

Mentions:
Pioneering studies on microbiota in clouds have shown the presence of prevalent bacteria that are common with phyllosphere microbiota, thus suggesting that at least some epiphytic microorganisms are adapted to the conditions of the troposphere (DeLeon-Rodriguez et al., 2013; Šantl-Temkiv et al., 2013). Tropospheric microorganisms are likely to act as water condensation or nucleation centers during cloud formation and to be involved in global carbon cycles through metabolization of the organic compounds that are present in clouds (Vaïtilingom et al., 2013). Moreover, epiphytic microorganisms may constitute the major source of airborne bacteria, including ice nucleation-active (INA) bacteria. These bacteria mainly belong to the order of Gammaproteobacteria and possess common INA proteins encoded by ina genes that were qPCR quantified and estimated to reach up to 108ina genes per g of fresh weight in the foliage of cereals (Lindemann et al., 1982; Hill et al., 2014). The presence of INA proteins may also contribute to bacteria dissemination processes via deposition on cloud droplets. There may thus be strong links between phyllosphere microbiota and cloud microbiota (Figure 5) with important implications for climate regulation.

Bottom Line:
The phyllosphere, which lato sensu consists of the aerial parts of plants, and therefore primarily, of the set of photosynthetic leaves, is one of the most prevalent microbial habitats on earth.Recent -omics studies have opened fascinating opportunities for characterizing the spatio-temporal structure of phyllosphere microbial communities in relation with structural, functional, and ecological properties of host plants, and with physico-chemical properties of the environment, such as climate dynamics and trace gas composition of the surrounding atmosphere.This review will analyze recent advances, especially those resulting from environmental genomics, and how this novel knowledge has revealed the extent of the ecosystemic impact of the phyllosphere at the interface between plants and atmosphere.

ABSTRACTThe phyllosphere, which lato sensu consists of the aerial parts of plants, and therefore primarily, of the set of photosynthetic leaves, is one of the most prevalent microbial habitats on earth. Phyllosphere microbiota are related to original and specific processes at the interface between plants, microorganisms and the atmosphere. Recent -omics studies have opened fascinating opportunities for characterizing the spatio-temporal structure of phyllosphere microbial communities in relation with structural, functional, and ecological properties of host plants, and with physico-chemical properties of the environment, such as climate dynamics and trace gas composition of the surrounding atmosphere. This review will analyze recent advances, especially those resulting from environmental genomics, and how this novel knowledge has revealed the extent of the ecosystemic impact of the phyllosphere at the interface between plants and atmosphere. Highlights • The phyllosphere is one of the most prevalent microbial habitats on earth. • Phyllosphere microbiota colonize extreme, stressful, and changing environments. • Plants, phyllosphere microbiota and the atmosphere present a dynamic continuum. • Phyllosphere microbiota interact with the dynamics of volatile organic compounds and atmospheric trace gasses.